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Tracking transitional probabilities and segmenting auditory sequences are dissociable processes in adults and neonates

Benjamin, Lucas; Fló, Ana; Palu, Marie; Naik, Shruti; Melloni, Lucia; Dehaene-Lambertz, Ghislaine
Since speech is a continuous stream with no systematic boundaries between words, how do pre-verbal infants manage to discover words? A proposed solution is that they might use the transitional probability between adjacent syllables, which drops at word boundaries. Here, we tested the limits of this mechanism by increasing the size of the word-unit to four syllables, and its automaticity by testing asleep neonates. Using markers of statistical learning in neonates' EEG, compared to adult behavioral performances in the same task, we confirmed that statistical learning is automatic enough to be efficient even in sleeping neonates. We also revealed that: (1) Successfully tracking transition probabilities (TP) in a sequence is not sufficient to segment it. (2) Prosodic cues, as subtle as subliminal pauses, enable to recover words segmenting capacities. (3) Adults' and neonates' capacities to segment streams seem remarkably similar despite the difference of maturation and expertise. Finally, we observed that learning increased the overall similarity of neural responses across infants during exposure to the stream, providing a novel neural marker to monitor learning. Thus, from birth, infants are equipped with adult-like tools, allowing them to extract small coherent word-like units from auditory streams, based on the combination of statistical analyses and auditory parsing cues. RESEARCH HIGHLIGHTS: Successfully tracking transitional probabilities in a sequence is not always sufficient to segment it. Word segmentation solely based on transitional probability is limited to bi- or tri-syllabic elements. Prosodic cues, as subtle as subliminal pauses, enable to recover chunking capacities in sleeping neonates and awake adults for quadriplets.
PMID: 35772033
ISSN: 1467-7687
CID: 5281302

The ConTraSt database for analysing and comparing empirical studies of consciousness theories

Yaron, Itay; Melloni, Lucia; Pitts, Michael; Mudrik, Liad
Understanding how consciousness arises from neural activity remains one of the biggest challenges for neuroscience. Numerous theories have been proposed in recent years, each gaining independent empirical support. Currently, there is no comprehensive, quantitative and theory-neutral overview of the field that enables an evaluation of how theoretical frameworks interact with empirical research. We provide a bird's eye view of studies that interpreted their findings in light of at least one of four leading neuroscientific theories of consciousness (N = 412 experiments), asking how methodological choices of the researchers might affect the final conclusions. We found that supporting a specific theory can be predicted solely from methodological choices, irrespective of findings. Furthermore, most studies interpret their findings post hoc, rather than a priori testing critical predictions of the theories. Our results highlight challenges for the field and provide researchers with an open-access website ( https://ContrastDB.tau.ac.il ) to further analyse trends in the neuroscience of consciousness.
PMID: 35190711
ISSN: 2397-3374
CID: 5175042

Shared computational principles for language processing in humans and deep language models

Goldstein, Ariel; Zada, Zaid; Buchnik, Eliav; Schain, Mariano; Price, Amy; Aubrey, Bobbi; Nastase, Samuel A; Feder, Amir; Emanuel, Dotan; Cohen, Alon; Jansen, Aren; Gazula, Harshvardhan; Choe, Gina; Rao, Aditi; Kim, Catherine; Casto, Colton; Fanda, Lora; Doyle, Werner; Friedman, Daniel; Dugan, Patricia; Melloni, Lucia; Reichart, Roi; Devore, Sasha; Flinker, Adeen; Hasenfratz, Liat; Levy, Omer; Hassidim, Avinatan; Brenner, Michael; Matias, Yossi; Norman, Kenneth A; Devinsky, Orrin; Hasson, Uri
Departing from traditional linguistic models, advances in deep learning have resulted in a new type of predictive (autoregressive) deep language models (DLMs). Using a self-supervised next-word prediction task, these models generate appropriate linguistic responses in a given context. In the current study, nine participants listened to a 30-min podcast while their brain responses were recorded using electrocorticography (ECoG). We provide empirical evidence that the human brain and autoregressive DLMs share three fundamental computational principles as they process the same natural narrative: (1) both are engaged in continuous next-word prediction before word onset; (2) both match their pre-onset predictions to the incoming word to calculate post-onset surprise; (3) both rely on contextual embeddings to represent words in natural contexts. Together, our findings suggest that autoregressive DLMs provide a new and biologically feasible computational framework for studying the neural basis of language.
PMCID:8904253
PMID: 35260860
ISSN: 1546-1726
CID: 5190382

Event boundaries shape temporal organization of memory by resetting temporal context

Pu, Yi; Kong, Xiang-Zhen; Ranganath, Charan; Melloni, Lucia
In memory, our continuous experiences are broken up into discrete events. Boundaries between events are known to influence the temporal organization of memory. However, how and through which mechanism event boundaries shape temporal order memory (TOM) remains unknown. Across four experiments, we show that event boundaries exert a dual role: improving TOM for items within an event and impairing TOM for items across events. Decreasing event length in a list enhances TOM, but only for items at earlier local event positions, an effect we term the local primacy effect. A computational model, in which items are associated to a temporal context signal that drifts over time but resets at boundaries captures all behavioural results. Our findings provide a unified algorithmic mechanism for understanding how and why event boundaries affect TOM, reconciling a long-standing paradox of why both contextual similarity and dissimilarity promote TOM.
PMID: 35110527
ISSN: 2041-1723
CID: 5153662

On Keeping Our Adversaries Close, Preventing Collateral Damage, and Changing Our Minds

Melloni, Lucia
Disagreement is a powerful engine of scientific advance. It sharpens conceptual boundaries, directs attention to neglected issues, and, of course, prompts the design of would-be decisive experiments"”(Gilovich et al., 1998)
SCOPUS:85131320956
ISSN: 2211-3681
CID: 5314622

Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability

Iemi, Luca; Gwilliams, Laura; Samaha, Jason; Auksztulewicz, Ryszard; Cycowicz, Yael M; King, Jean-Remi; Nikulin, Vadim V; Thesen, Thomas; Doyle, Werner; Devinsky, Orrin; Schroeder, Charles E; Melloni, Lucia; Haegens, Saskia
The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Ongoing fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on intracranial electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.
PMID: 34875382
ISSN: 1095-9572
CID: 5105842

Long-term priors influence visual perception through recruitment of long-range feedback

Hardstone, Richard; Zhu, Michael; Flinker, Adeen; Melloni, Lucia; Devore, Sasha; Friedman, Daniel; Dugan, Patricia; Doyle, Werner K; Devinsky, Orrin; He, Biyu J
Perception results from the interplay of sensory input and prior knowledge. Despite behavioral evidence that long-term priors powerfully shape perception, the neural mechanisms underlying these interactions remain poorly understood. We obtained direct cortical recordings in neurosurgical patients as they viewed ambiguous images that elicit constant perceptual switching. We observe top-down influences from the temporal to occipital cortex, during the preferred percept that is congruent with the long-term prior. By contrast, stronger feedforward drive is observed during the non-preferred percept, consistent with a prediction error signal. A computational model based on hierarchical predictive coding and attractor networks reproduces all key experimental findings. These results suggest a pattern of large-scale information flow change underlying long-term priors' influence on perception and provide constraints on theories about long-term priors' influence on perception.
PMID: 34725348
ISSN: 2041-1723
CID: 5037932

Effects of hippocampal interictal discharge timing, duration, and spatial extent on list learning

Leeman-Markowski, Beth; Hardstone, Richard; Lohnas, Lynn; Cowen, Benjamin; Davachi, Lila; Doyle, Werner; Dugan, Patricia; Friedman, Daniel; Liu, Anli; Melloni, Lucia; Selesnick, Ivan; Wang, Binhuan; Meador, Kimford; Devinsky, Orrin
Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimental to memory, however, are undefined. We studied the impact of temporal and spatial characteristics of IEDs on list learning. Subjects completed a memory task during intracranial EEG recordings including hippocampal depth and temporal neocortical subdural electrodes. Subjects viewed a series of objects, and after a distracting task, recalled the objects from the list. The impacts of IED presence, duration, and propagation to neocortex during encoding of individual stimuli were assessed. The effects of IED total number and duration during maintenance and recall periods on delayed recall performance were also determined. The influence of IEDs during recall was further investigated by comparing the likelihood of IEDs preceding correctly recalled items vs. periods of no verbal response. Across 6 subjects, we analyzed 28 hippocampal and 139 lateral temporal contacts. Recall performance was poor, with a median of 17.2% correct responses (range 10.4-21.9%). Interictal epileptiform discharges during encoding, maintenance, and recall did not significantly impact task performance, and there was no significant difference between the likelihood of IEDs during correct recall vs. periods of no response. No significant effects of discharge duration during encoding, maintenance, or recall were observed. Interictal epileptiform discharges with spread to lateral temporal cortex during encoding did not adversely impact recall. A post hoc analysis refining model assumptions indicated a negative impact of IED count during the maintenance period, but otherwise confirmed the above results. Our findings suggest no major effect of hippocampal IEDs on list learning, but study limitations, such as baseline hippocampal dysfunction, should be considered. The impact of IEDs during the maintenance period may be a focus of future research.
PMID: 34416521
ISSN: 1525-5069
CID: 4988992

Decoding the Content of Auditory Sensory Memory Across Species

Cappotto, Drew; Auksztulewicz, Ryszard; Kang, HiJee; Poeppel, David; Melloni, Lucia; Schnupp, Jan
In contrast to classical views of working memory (WM) maintenance, recent research investigating activity-silent neural states has demonstrated that persistent neural activity in sensory cortices is not necessary for active maintenance of information in WM. Previous studies in humans have measured putative memory representations indirectly, by decoding memory contents from neural activity evoked by a neutral impulse stimulus. However, it is unclear whether memory contents can also be decoded in different species and attentional conditions. Here, we employ a cross-species approach to test whether auditory memory contents can be decoded from electrophysiological signals recorded in different species. Awake human volunteers (N = 21) were exposed to auditory pure tone and noise burst stimuli during an auditory sensory memory task using electroencephalography. In a closely matching paradigm, anesthetized female rats (N = 5) were exposed to comparable stimuli while neural activity was recorded using electrocorticography from the auditory cortex. In both species, the acoustic frequency could be decoded from neural activity evoked by pure tones as well as neutral frozen noise burst stimuli. This finding demonstrates that memory contents can be decoded in different species and different states using homologous methods, suggesting that the mechanisms of sensory memory encoding are evolutionarily conserved across species.
PMID: 33625488
ISSN: 1460-2199
CID: 4794692

Making the hard problem of consciousness easier

Melloni, Lucia; Mudrik, Liad; Pitts, Michael; Koch, Christof
PMID: 34045342
ISSN: 1095-9203
CID: 4924342